After working after graduation as a reporter for the newspaper in Springfield, Massachusetts owned by his family, Bowles took a minor position with the United States consulate in Shanghai, but soon returned to the U.S. because of his father's illness.

Bowles became an copywriter for $25 per week at the Batten Company, an advertising agency in New York City that later became BBDO, the third-largest agency in the USA.

In 1929, Bowles established the Benton & Bowles advertising agency with William Benton, who was a fellow Batten employee. Despite the difficult economic environment of Great Depression, by the mid-1930s Benton & Bowles was a multimillion-dollar company. Benton & Bowles created the radio soap opera, offering specialized programming to receptive demographic groups. This allowed Benton & Bowles to create advertising campaigns to promote their clients' products to this targeted radio audience.

Bowles was appointed chairman of the board in 1936. By 1941, the company reportedly earned an annual profit of more than $250,000. Bowles sold his shares in Benton & Bowles for a substantial profit. He became a multi-millionaire who retired the first time by age 40.

Benton & Bowles merged to become D'arcy, Macius, Benton & Bowles in 1986. It merged with Leo Burnett in 1999. The combined agency, which continues to be known as Leo Burnett, was purchased by Publicis in 2002, the world's third-largest marketing and advertising firm, based on 2015 revenues.[2][3]

Because of his strong support for the New Deal policies of the Roosevelt Administration, Bowles worked closely with First Lady Eleanor Roosevelt on several key policy initiatives and programs, while continuing his work at Benton & Bowles.[4]

Initially, Bowles was opposed to the United States getting involved in World War II and joined an opposition group, the America First Committee. Later, he said he was embarrassed by his views, and he soon became a supporter of U.S. involvement in the war.

When the United States entered World War II in December 1941, he attempted to join the Navy. Bowles was rejected because of an earlier injury to his ear.

Bowles then took a job as the state of Connecticut's rationing administrator in 1942. He becoming state director of price administration later that year, and then general manager. He was appointed by President Roosevelt in 1943 as administrator of the Office of Price Administration and served in that position until 1946. He served as a member of the War Production Board and the Petroleum Board for War.[5]

He continued with the United Nations as International Chairman of the United Nations Children's Appeal from 1948 to 1951.

Bowles was elected to the governorship of Connecticut in 1948, defeating James C. Shannon, and served one term, during which time he signed into law an end to segregation in the state national guard. During his term, Bowles was also active in improving education, mental health, housing and workmen's compensation. His liberal views and policies while governor are attributed by most as the primary reason he lost his re-election bid in 1950.

Bowles ran for and won a seat in the House of Representatives for Connecticut's second district and served one term, from January 3, 1959 to January 3, 1961.[7] He lost a bitter re-election campaign to John Davis Lodge, during which his opponent painted him as an extreme liberal.

Bowles at his 1961 swearing in as President Kennedy's Special Representative.

That November, Bowles was removed as a consequence of the perception in the Kennedy Administration that he failed to carry out key duties as an administrator in the Department of State, and because he leaked his opposition to the Bay of Pigs Invasion. His removal was made part of a broader bureaucratic reshuffle, which became known as the "Thanksgiving Day Massacre". In early December 1961, he was replaced by George Ball as Under Secretary.

In December 1961, Bowles was named President Kennedy's Special Representative and Adviser on African, Asian, and Latin American Affairs, and Ambassador at Large. Ostensibly this new position was a promotion, but this job was recognized by most experts involved at the time (and by historians in later years) as a demotion designed to reduce public embarrassment for Bowles and the Administration regarding Bowles's removal from the Under Secretary position.

Bowles was made Ambassador to India for the second time on July 19, 1963. He continued in this position through the remainder of Kennedy's Presidency, and for the duration of Lyndon B. Johnson's Administration.

Bowles was a passionate advocate for stronger relations between the United States and India. He enjoyed good relations with India's first prime minister, Jawaharlal Nehru. Bowles strongly believed that the United States and India shared fundamental democratic values.

In March 1967, Bowles was formally petitioned for political asylum by Svetlana Alliluyeva, a writer and the only daughter of Soviet leader Joseph Stalin, which was granted. Bowles arranged for her to leave India immediately on a middle-of-the-night flight to Rome. She traveled to Switzerland and eventually on to the U.S., where she died in 2011.

Bowles completed his service as Ambassador to India on April 21, 1969, during the early days of the presidency of Richard Nixon.

Chester Bowles was well-known for his oft-repeated phrase, that he always had "a feeling for the people's side." He said that his grandfather and great-grandfather also used that phrase in their careers in journalism as newspaper owners.[8] Bowles showed expertise in stagecraft, public relations and promotion, both during his career in advertising, and throughout his work as a diplomat, elected official and appointed official. For many years he was a successful author and lecturer, giving him platforms to promote his beliefs and views of politics, policy and the quest for peace.

Early on, while a student at Yale College, his goal was to join the United States foreign service to become a career diplomat. Even while a business executive in the late 1920s and throughout the 1930s, he fostered a keen, growing interest in domestic issues, international issues, and a wide array of other political issues of the day. With the election of Franklin Roosevelt to the presidency in 1932, Bowles saw in the New Deal policies many ideas and concepts that he liked and would promote for decades.[9]

Because of the strength and wealth of the United States, Bowles believed that it was essential for America to further develop vigorous, sizable foreign aid programs to a large number of countries.

Bowles was a long-time advocate for peace. Because of that deep-rooted sense that peace was vital to survival and happiness of the world's population, Bowles was opposed to the Vietnam War and to the involvement of the United States in Southeast Asia.

European reconstruction was vital, he believed, after the massive devastation of World War II. That devastation was due in no small measure to the bombing and other military activities conducted by the USA and its Allies over the years of conflict in Europe, in his view. Bowles understood that the Nazi regime of Germany - and others in Axis alliance - needed to be defeated. Yet that meant destruction of buildings, infrastructure, deaths of civilians. Shortly after the war, Bowles saw the hampered abilities of the countries to produce food, clothe their people, provide education, sanitation and health care. Jobs were scarce and opportunities were limited for most people. Yet he was convinced that after the war the United States had a moral obligation to assist with the re-building of affected countries and with meeting the humanitarian needs of the affected people.

Civil rights was of paramount importance to Chester Bowles. As a white liberal from the Northeast, he used various tools to foment change that encouraged the independence, freedom and equality for African-Americans and other minorities, supporting changes in the laws advocating for enlightened judicial decisions affecting civil rights. He wrote articles and books that promoted civil rights and agitation for change and improvement, including in a book entitled "What Negroes Can Learn from Gandhi" published in 1958. He advanced these rights by supporting various government programs and private philanthropic initiatives.

Bowles had two children (Chester and Barbara) with his first wife, the former Julia Fisk. He was married to Fisk in 1925. They divorced in 1933.

Bowles had three children (Cynthia, Sally, and Sam) with his second wife, the former Dorothy Stebbens. He married Stebbens in 1934.[10] Daughter Sally Bowles continued her father's tradition of public service,[11] Chester Jr. is an architect, and Samuel Bowles is a well-known economist.

Bowles died at the age of 85, on May 25, 1986 in Essex, Connecticut. He struggled with Parkinson's disease for 22 years (diagnosed when he was Ambassador to India). He also had a cerebrovascular accident (a stroke) the week prior to his death.[12] He is buried there in River View Cemetery.[13]